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Reactive oxygen species trigger the fast action of glufosinate

  • Hudson K. Takano
  • Roland Beffa
  • Christopher Preston
  • Philip Westra
  • Franck E. DayanEmail author
Original Article
  • 107 Downloads

Abstract

Main conclusion

Glufosinate is primarily toxic to plants due to a massive light-dependent generation of reactive oxygen species rather than ammonia accumulation or carbon assimilation inhibition.

Glutamine synthetase (GS) plays a key role in plant nitrogen metabolism and photorespiration. Glufosinate (C5H12NO4P) targets GS and causes catastrophic consequences leading to rapid plant cell death, and the causes for phytoxicity have been attributed to ammonia accumulation and carbon assimilation restriction. This study aimed to examine the biochemical and physiological consequences of GS inhibition to identify the actual cause for rapid phytotoxicity. Monocotyledonous and dicotyledonous species with different forms of carbon assimilation (C3 versus C4) were selected as model plants. Glufosinate sensitivity was proportional to the uptake of herbicide between species. Herbicide uptake also correlated with the level of GS inhibition and ammonia accumulation in planta even with all species having the same levels of enzyme sensitivity in vitro. Depletion of both glutamine and glutamate occurred in glufosinate-treated leaves; however, amino acid starvation would be expected to cause a slow plant response. Ammonia accumulation in response to GS inhibition, often reported as the driver of glufosinate phytotoxicity, occurred in all species, but did not correlate with either reductions in carbon assimilation or cell death. This is supported by the fact that plants can accumulate high levels of ammonia but show low inhibition of carbon assimilation and absence of phytotoxicity. Glufosinate-treated plants showed a massive light-dependent generation of reactive oxygen species, followed by malondialdehyde accumulation. Consequently, we propose that glufosinate is toxic to plants not because of ammonia accumulation nor carbon assimilation inhibition, but the production of reactive oxygen species driving the catastrophic lipid peroxidation of the cell membranes and rapid cell death.

Keywords

Glutamine synthetase Phosphinothricin Ammonia accumulation Photosynthesis Light dependent Lipid peroxidation 

Notes

Acknowledgements

We thank Bayer CropScience for funding this research.

Compliance with ethical standards

Conflict of interest

We declare no conflict of interest.

Supplementary material

425_2019_3124_MOESM1_ESM.docx (16 kb)
Supplementary material 1 (DOCX 16 kb)
425_2019_3124_MOESM2_ESM.eps (132 kb)
Supplementary material 2 (EPS 132 kb) Supplementary Fig. S1. Total ion chromatogram from the LC–MS/MS analysis for glufosinate-treated (A) and glufosinate-untreated (B) palmer amaranth plants
425_2019_3124_MOESM3_ESM.eps (122 kb)
Supplementary material 3 (EPS 121 kb)
425_2019_3124_MOESM4_ESM.eps (123 kb)
Supplementary material 4 (EPS 123 kb) Supplementary Fig. S2. Ammonia accumulation overtime after glufosinate application in horseweed, palmer amaranth, kochia, ryegrass and johnsongrass
425_2019_3124_MOESM5_ESM.eps (92 kb)
Supplementary material 5 (EPS 92 kb) Supplementary Fig. S3. Visual injury and ammonia accumulation in glufosinate-treated plants growing in water or 10 mM glutamine at 8 HAT

References

  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  2. Bayer E, Gugel KH, Hägele K, Hagenmaier H, Jassipow S, König WA, Zähner H (1972) Stoffwechselprodukte von mikroorganismen. Phosphinothricin und phosphinothricyl-alanyl-alanin. Helv Chim Acta 55:224–239CrossRefGoogle Scholar
  3. Bernard SM, Habash DZ (2009) The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 182:608–620CrossRefGoogle Scholar
  4. Blackwell RD, Murray AJS, Lea PJ (1987) Inhibition of photosynthesis in barley with decreased levels of chloroplastic glutamine synthetase activity. J Exp Bot 38:1799–1809CrossRefGoogle Scholar
  5. Blackwell RD, Murray AJS, Lea PJ, Kendall AC, Hall NP, Turner JC, Wallsgrove RM (1988) The value of mutants unable to carry out photorespiration. Photosynth Res 16:155–176CrossRefGoogle Scholar
  6. Coetzer E, Al-Khatib K (2001) Photosynthetic inhibition and ammonium accumulation in Palmer amaranth after glufosinate application. Weed Sci 49:454–459CrossRefGoogle Scholar
  7. Culpepper AS, York AC, Batts RB, Jennings KM (2000) Weed management in glufosinate- and glyphosate-resistant soybean (Glycine max). Weed Technol 14:77–88CrossRefGoogle Scholar
  8. Dayan FE, Duke SO (2014) Natural compounds as next generation herbicides. Plant Physiol 166:1090–1105CrossRefGoogle Scholar
  9. Dayan FE, Owens DK, Corniani N, Silva FML, Watson SB, Howell JL, Shaner DL (2015) Biochemical markers and enzyme assays for herbicide mode of action and resistance studies. Weed Sci 63:23–63CrossRefGoogle Scholar
  10. Dayan FE, Barker A, Dayan L, Ravet K (2019) The role of antioxidants in the protection of plants against inhibitors of protoporphyrinogen oxidase. Reac Oxyg Species 7:55–63Google Scholar
  11. Douce R, Bourguignon J, Neuburger M, Rébeillé F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6:167–176CrossRefGoogle Scholar
  12. Duke SO, Powles SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64:319–325CrossRefGoogle Scholar
  13. Edwards JW, Walker EL, Coruzzi GM (1990) Cell-specific expression in transgenic plants reveals nonoverlapping roles for chloroplast and cytosolic glutamine synthetase. Proc Natl Acad Sci USA 87:3459–3463CrossRefGoogle Scholar
  14. Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot 58:2339–2358CrossRefGoogle Scholar
  15. Forlani G (2000) Purification and properties of a cytosolic glutamine synthetase expressed in Nicotiana plumbaginifolia cultured cells. Plant Physiol Biochem 38:201–207CrossRefGoogle Scholar
  16. Frantz TA, Peterson DM, Durbin RD (1982) Sources of ammonium in oat leaves treated with tabtoxin or methionine sulfoximine. Plant Physiol 69:345–348CrossRefGoogle Scholar
  17. Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254Google Scholar
  18. Gill HS, Eisenberg D (2001) The crystal structure of phosphinothricin in the active site of glutamine synthetase illuminates the mechanism of enzymatic inhibition. Biochemistry 40:1903–1912CrossRefGoogle Scholar
  19. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  20. Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611CrossRefGoogle Scholar
  21. Izawa S (1977) Inhibition of electron transport. In: Trebst A, Avron M (eds) Encyclopedia of plant physiology. Springer, Berlin, pp 266–279Google Scholar
  22. Johansson L, Larsson C-M (1986) Relationship between inhibition of CO2 fixation and glutamine synthetase inactivation in Lemna gibba L. treated with l-methionine-d, l-sulphoximine (MSO). J Exp Bot 37:221–229CrossRefGoogle Scholar
  23. Kamachi K, Yamaya T, Hayakawa T, Mae T, Ojima K (1992) Vascular bundle-specific localization of cytosolic glutamine synthetase in rice leaves. Plant Physiol 99:1481–1486CrossRefGoogle Scholar
  24. Krieg LC, Walker MA, Senaratna T, McKersie BD (1990) Growth, ammonia accumulation and glutamine synthetase activity in alfalfa (Medicago sativa L.) shoots and cell cultures treated with phosphinothricin. Plant Cell Rep 9:80–83CrossRefGoogle Scholar
  25. Kumaratilake AR, Lorraine-Colwill DF, Preston C (2002) A comparative study of glufosinate efficacy in rigid ryegrass (Lolium rigidum) and sterile oat (Avena sterilis). Weed Sci 50:560–566CrossRefGoogle Scholar
  26. Lu Y, Li Y, Yang Q, Zhang Z, Chen Y, Zhang S, Peng X-X (2014) Suppression of glycolate oxidase causes glyoxylate accumulation that inhibits photosynthesis through deactivating Rubisco in rice. Physiol Plant 150:463–476CrossRefGoogle Scholar
  27. Manderscheid R, Wild A (1986) Studies on the mechanism of inhibition by phosphinothricin of glutamine synthetase isolated from Triticum aestivum L. J Plant Physiol 123:135–142CrossRefGoogle Scholar
  28. McNally SF, Hirel B, Stewart GR (1983) Nitrogen metabolism in halophytes 5. The occurence of multiple forms of glutamine synthetase in leaf tissue. New Phytol 94:47–56CrossRefGoogle Scholar
  29. Miflin BJ, Lea PJ (1976) The pathway of nitrogen assimilation in plants. Phytochem 15:873–885CrossRefGoogle Scholar
  30. Molin WT, Khan RA (1995) Microbioassays to determine the activity of membrane disrupter herbicides. Pestic Biochem Physiol 53:172–179CrossRefGoogle Scholar
  31. Ridley SM, McNally SF (1985) Effects of phosphinothricin on the isoenzymes of glutamine synthetase isolated from plant species which exhibit varying degrees of susceptibility to the herbicide. Plant Sci 39:31–36CrossRefGoogle Scholar
  32. Sauer H, Wild A, Rühle W (1987) The effect of phosphinothricin (glufosinate) on photosynthesis II. The causes of inhibition of photosynthesis. Z Naturforsch 42C:270–278CrossRefGoogle Scholar
  33. Shaner DL (2014) Herbicide handbook, 10th edn. Weed Science Society of America, Lawrence, KSGoogle Scholar
  34. Thomsen HC, Eriksson D, Møller IS, Schjoerring JK (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci 19(10):656–663CrossRefGoogle Scholar
  35. Wallsgrove RM, Turner JC, Hall NP, Kendall AC, Bright SW (1987) Barley mutants lacking chloroplast glutamine synthetase-biochemical and genetic analysis. Plant Physiol 83:155–158CrossRefGoogle Scholar
  36. Wendler C, Barniske M, Wild A (1990) Effect of phosphinothricin (glufosinate) on photosynthesis and photorespiration of C3 and C4 plants. Photosynth Res 24:55–61CrossRefGoogle Scholar
  37. Wendler C, Putzer A, Wild A (1992) Effect of glufosinate (phosphinothricin) and inhibitors of photorespiration on photosynthesis and ribulose-1,5-bisphosphate carboxylase activity. J Plant Physiol 139:666–671CrossRefGoogle Scholar
  38. Whitcomb CE (1999) An introduction to ALS-inhibiting herbicides. Toxicol Ind Health 15:232–240CrossRefGoogle Scholar
  39. Wild A, Sauer H, Ruhle W (1987) The effect of phosphinothricin (glufosinate) on photosynthesis. I. Inhibition of photosynthesis and accumulation of ammonia. Z Naturforsch 42C:263–269CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Bioagricultural Sciences and Pest ManagementColorado State UniversityFort CollinsUSA
  2. 2.Weed Resistance Research Centre, Bayer AG, Industriepark HoechstFrankfurtGermany
  3. 3.School of Agriculture, Food and WineUniversity of AdelaideAdelaideAustralia

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